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Review Article | Thoracic Imaging

https://doi.org/10.3348/kjr.2018.19.5.866
pISSN 1229-6929 · eISSN 2005-8330
Korean J Radiol 2018;19(5):866-871

2018 Korean Clinical Imaging Guideline for Hemoptysis


Mi-Jin Kang, MD1, Jin Hwan Kim, MD, PhD2, Yoon Kyung Kim, MD, PhD3, Hyun Joo Lee, MD4,
Kyung Min Shin, MD5, Jung Im Kim, MD, PhD6, Hyun Ju Lee, MD, PhD7, Kyung Hyun Do, MD, PhD4,
Hwan Seok Yong, MD, PhD8, Sol Ji Choi, PhD9, Miyoung Choi, RN, MPH, PhD9, Jung Im Jung, MD, PhD10
1
Department of Radiolgoy, InJe University Sanggye Paik Hospital, Seoul 01757, Korea; 2Department of Radiology, Chungnam National University
Hospital, Chungnam National University School of Medicine, Daejeon 35015, Korea; 3Department of Radiology, Gachon University Gil Hospital,
Incheon 21565, Korea; 4Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical
Center, Seoul 05505, Korea; 5Department of Radiology, Kyungpook National University Medical Center, Daegu 41944, Korea; 6Department of
Radiology, Kyung Hee University Hospital at Gangdong, Kyung Hee University College of Medicine, Seoul 05278, Korea; 7Department of Radiology,
Seoul National University Hospital, Seoul 03080, Korea; 8Department of Radiology, Korea University Guro Hospital, Korea University College of
Medicine, Seoul 08308, Korea; 9Division for Healthcare Technology Assessment Research, National Evidence-based Healthcare Collaborating
Agency, Seoul 04554, Korea; 10Department of Radiology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul
06591, Korea

In 2014, the American College of Radiology (ACR) announced the guideline for the appropriate diagnostic approach and
treatment of patients according to the severity of hemoptysis and risk for lung cancer. However, the application of the ACR
guideline in Korea may not be appropriate, because many patients in Korea have active tuberculosis or pulmonary fibrosis
due to previous tuberculosis. The Korean Society of Radiology and Korean Society of Thoracic Radiology have proposed a
new guideline suitable for Korean practice. This new guideline was prepared through the consensus of a development
committee, working party, and an advisory committee. The guideline proposal process was based on an evidence-based
clinical imaging guideline proposed by the development committee. Clinical imaging guideline for adult patients with
hemoptysis is as follows: Chest radiography is an initial imaging modality to evaluate hemoptysis. Contrast-enhanced chest
CT is recommended in patients with two risk factors for lung cancer (> 40 years old and > 30 pack-year smoking history),
moderate hemoptysis (> 30 mL/24 hours) or recurrent hemoptysis. Contrast-enhanced chest CT is also recommended in
patients with massive hemoptysis (> 400 mL/24 hours) without cardiopulmonary compromise.
Keywords: Guideline; Hemoptysis; Thorax; Lung; Radiography; X-ray; Computed tomography; Evidence; Republic of Korea

Received February 22, 2018; accepted after revision April 3, 2018.


This study was supported by the National Evidence-based Collaborating Agency (NECA-C-15-003) and the Korean Society of Radiology
(NECA-S-15-002).
This Guideline has been published jointly by invitation and consent in both the Journal of the Korean Society of Radiology (in Korean)
and the Korean Journal of Radiology (in English).
Corresponding author: Jung Im Jung, MD, PhD, Department of Radiology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic
University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 06591, Korea.
• Tel: (822) 2258-1435 • Fax: (822) 599-6771 • E-mail: jijung@catholic.ac.kr
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://
creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium,
provided the original work is properly cited.

866 Copyright © 2018 The Korean Society of Radiology


Clinical Imaging Guideline for Hemoptysis

Background of the Development of the Korean tuberculosis. Consequently, the development committee,
Clinical Imaging Guideline working party, and an advisory committee have developed a
guideline suitable for Korean practice.
Hemoptysis is the expectoration of blood to mouth or
nose that originates from the respiratory tract. Clinical Adaptation Process of the Guidelines
management is different according to the severity of
hemoptysis based on the volume of blood loss. However, The guideline development process was based on a
retained blood in lung parenchyma can be underestimated guideline adaptation methodology process suggested by the
due to the difficulty in determining the exact volume of development committee (2).
blood loss in routine practice. Diagnostic imaging is salient
for appropriate diagnosis and treatment because hemoptysis Key Questions
can originate from various diseases such as acute benign The key questions made by working group were reviewed
disease (including bronchitis), chronic benign disease and revised by the development committee and consensus
(including bronchiectasis), or malignant tumor. group. The consensus group represented the suggested
A clinical imaging guideline for hemoptysis has been end user and was selected from The Korean Academy of
previously published by the American College of Radiology Tuberculosis and Respiratory Disease. The finalized key
(ACR) (1). ACR guideline states diagnostic and treatment question is in a structured form below.
strategies according to the severity of hemoptysis and risk 1. What is the most appropriate imaging test to
factor for lung cancer. The ACR emphasized the importance diagnose the cause of hemoptysis in an adult patient with
of undiagnosed lung cancer in hemoptysis patients. hemoptysis?
However, there is a need for a guideline specific to
Korea, because it is an endemic tuberculosis area with a Search Guidelines
high rate of hemoptysis patients with pulmonary fibrosis The development committee searched for guidelines
caused by previous tuberculosis or hemoptysis from active using international databases (Ovid-MEDLINE and Ovid-

Records identified through international database searching Records identified through domestic database searching
Ovid-MEDLINE (n = 4) KoreaMed (n = 4)
Ovid-EMBASE (n = 13) KMBASE (n = 1)
NGC (n = 9) KGC (n = 9)
GIN (n = 6) KoMGI (n = 0)
Trip OR Google (n = 0) Searched guideline through manual method (n = 1)
(Total n = 32) (Total n = 15)

Records after duplication removed


Records excluded by abstract screening
(domestic n = 15/international n = 32)
(Total n = 26)
(Total n = 47)

Full-text guidelines assessed for eligibility Records excluded according to exclusion criteria (n = 20)
(domestic n = 0/international n = 21) 1. Patients of hemoptysis are not included (n = 10)
(Total n = 21) 2. Guidelines not related to hemoptysis (n = 8)
3. Appropriate results were not reported (n = 1)
4. Recommendations were not suggested (n = 0)
5. Guidelines not reported in English or Korean (n = 1)
6. Overlapping publication (n = 0)
7. Full-text was not obtainable (n = 0)
Guidelines included for KCIG
(domestic n = 0/international n = 1)
(Total n = 1)

Fig. 1. Flow chart for literature selection. GIN = Guideline International Network, KCIG = Korean Clinical Imaging Guidelines, KGC = Korean
Guideline Clearinghouse, KoMGI = Korean Medical Guidelines and Information, NGC = National Guideline Clearinghouse

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Kang et al.

Table 1. AGREE II
Source of Recommendation AGREE II Score Proposal of Developmental Committee
ACR Appropriateness Criteria® hemoptysis 66 Recommended
Not recommended: AGREE score < 50. ACR = American College of Radiology, AGREE II = Appraisal of Guidelines for Research & Evaluation II

Table 2. Criteria for Evidence Level of Each Evidence Literature


Level Content
Research satisfying all of criteria following three
1) Good reference standard
2) Consecutive patients study
1
3) Blind interpretation
Systematic review of level 1
Randomized controlled trial or cross-sectional cohort study that compares index test to comparators
Research satisfying all of criteria following two
1) Good reference standard
2 2) Consecutive patients study or blind interpretation
Systematic review of level 2
Observational studies that compares index test to comparators
3 Without consistently applied reference standards
Case-control study
4
Poor or non-independent reference standard
5 Expert opinion
Adapted from Choi et al. Korean J Radiol 2017;18:208-216 (2)

Table 3. Grades of Korean Clinical Imaging Guideline Recommendation


Grading Content Meaning
This intervention (examination) has enough evidence to support desired effect, and therefore, is
A Recommended
recommended
(Conditional) This intervention (examination) has intermediate to enough level of evidence to support desired effect
B
recommended Provide intervention (examination) selectively, or for specific individuals based on expert’s judgment
This intervention (examination) has enough evidence to support non-desired effect, and therefore, is not
C Not recommended
recommended (use of this examination is not recommended)
This intervention (examination) does not have enough evidence to either support or reject effectiveness,
and needs further research
I No recommendation
This intervention (examination) has very low level of certainty for desired effect, and decision based on
recommendation grading has no meaning
Adapted from Choi et al. Korean J Radiol 2017;18:208-216 (2)

EMBASE), several international sites associated with were included by an up-to-dated search.
guidelines (National Guideline Clearinghouse and Guideline
International Network) and major domestic databases Selection of Searched Guidelines
(KoreaMed, KMbase, Korean Medical Guidelines and A total of 47 guidelines were searched: 32 guidelines
Information, and Korean Guideline Clearinghouse). in an international database, 14 guidelines in a domestic
In addition, the websites of major academic societies database, and 1 guideline by a manual search. In the
and institutions were also searched along with a manual primary screening process, 21 records were selected after
database search. We performed literature searches reviewing the title and abstract of an identified study or
from 2000 to July, 2015 for the keywords hemoptysis, guideline. One guideline was selected after the full-texts
computerized tomography, or bronchoscopy, using Medical of identified literature were reviewed in the secondary
Subject Heading (MeSH) terms or Embase subject headings screening process that also noted the reason for the
(EMTREE). Guidelines or articles published after that period exclusion of any specific literature selected (Fig 1).

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Clinical Imaging Guideline for Hemoptysis

Quality Appraisal of the Guidelines Recommendations


The final selected guidelines underwent quality appraisal
using the Korean Appraisal of Guidelines for Research Key Question
& Evaluation II (AGREE II) tool of the development 1. What is the most appropriate imaging test to
committee. Final appraisal results were provided to the diagnose the cause of hemoptysis in an adult patient with
working group (Table 1). The working group selected one hemoptysis?
guideline for the key question in consideration of the
quality of the selected guideline. [Recommendation 1-1]
Chest radiography is suggested for initial evaluation in all
Grading the Level of Evidence and Drafting the adult patients with hemoptysis.
Recommendation Document (recommendation grade A, evidence level II)
Working group members reviewed evidence in the
literature that supported the final selected guideline [Recommendation 1-2]
recommendations. Grading the level of evidence for each Contrast-enhanced chest CT scan is recommended to
literature was performed to create an evidence table diagnose the cause of hemoptysis in all adult patients with
(Supplementary Table 1 in the online-only Data Supplement) hemoptysis and who have two risk factors for lung cancer (>
according to the evidence level criteria of the Korean 40 years old and > 30 pack-year smoking history).
Clinical Imaging Guidelines (K-CIG) (Tables 2, 3). The draft (recommendation grade A, evidence level II)
version of the recommendation document was based on
the prepared evidence table after a final discussion of the [Recommendation 1-3]
working group. Contrast-enhanced chest CT scan is recommended to
diagnose the cause of hemoptysis in all adult patients
Agreement of the Recommendation Grades with moderate hemoptysis (> 30 mL/24 hours) or recurrent
The draft version of the recommendation document hemoptysis.
prepared by the working group was reviewed and discussed (recommendation grade A, evidence level II)
by the development committee. The final level of evidence
and grade of recommendation was determined by the [Recommendation 1-4]
consensus of the development committee and working Contrast-enhanced chest CT scan should also be
group, according to K-CIG criteria (2). considered in adult patients with massive hemoptysis (>
400 mL/24 hours) and preserved cardiopulmonary function.
Finalizing the Recommendation Document (recommendation grade A, evidence level III)
The Delphi method was used for formal consensus. The
consensus group was composed of clinical imaging experts, Evidence Summary
end-users from the clinical imaging guideline-related Hemoptysis is spitting blood from the respiratory tract
academic societies (The Korean Academy of Tuberculosis and due to various causes that range from blood tinged sputum
Respiratory Disease), and research methodology experts. to massive hemoptysis. Causes of hemoptysis include benign
The results of the Delphi were as follows: degree of disease such as bronchiectasis, acute bronchitis, chronic
agreement on primary survey was 7.3−8.6 (standard bronchitis, tuberculosis, diffuse interstitial lung disease,
deviation: 0.5−0.9) and degree of agreement on secondary and pulmonary venous malformation or malignant disease
survey 6.9−8.5 (standard deviation: 0.5−0.8). such as lung cancer and idiopathic. Therefore, appropriate
screening test and complete medical examinations are
External Review and Approval of Clinical Guideline required (3-5). This paper proposes a clinical imaging
Clinical experts related to the area of the guideline for adult patients with hemoptysis.
recommendations, such as members from The Korean The guideline recommends chest radiography as an
Academy of Tuberculosis and Respiratory Disease reviewed initial evaluation for all adult hemoptysis patients. Chest
the final recommendations. Feedback and modification was radiography can help lateralize the bleeding site and screen
subsequently reflected in the documents. for the presence or absence of abnormality in the pleura

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Kang et al.

and lung parenchyma (3, 6, 7). embolization; however, moderate hemoptysis or mild but
Clinical imaging guidelines differ according to the amount chronic and worsening hemoptysis is also considered an
of hemoptysis: minor (< 30 mL/24 hours), moderate (30−400 indication of bronchial artery embolization (14). Contrast-
mL/24 hours), or massive hemoptysis (> 400 mL/24 hours) enhanced CT can guide bronchial artery embolization and
(7-10). reduce procedure time, because it adequately depicts the
Contrast-enhanced chest CT scan is recommended to imaging anatomy of the bronchial artery and non-bronchial
exclude the possibility of lung cancer in patients with collateral arteries (intercostal artery, subclavian artery,
hemoptysis and normal chest radiographs, if the patient axillary artery, and inferior phrenic artery), pulmonary
has two risk factors for malignancy (> 40 years old and artery and pulmonary vein (16).
> 30 pack-year smoking history). In adult patients with A contrast-enhanced CT scan is recommended for patients
hemoptysis, the incidence of malignancy was reported as with massive hemoptysis (> 400 mL/24 hours) who preserve
10−35% (2, 3). In a report on the long-term outcome and cardiopulmonary function. Massive hemoptysis can be
incidence of lung cancer in patients with hemoptysis of treated by bronchial artery embolization or surgery; in
unknown origin, unresectable lung cancer developed in 6% addition, CT prior to these treatments can be helpful to
of patients within 3 years after the first presentation; all detect the causative vessel (7, 17).
patients were smokers and > 40 years old (11). In another
retrospective study of patients with hemoptysis and normal Consideration for Recommendation
radiography, 9.6% of patients were diagnosed with lung
cancer; all patients were current or ex-smokers (12). Benefit and Harm
The accurate assessment of the cause is more important Performing chest radiography as a screening test in
than prompt treatment in patients with moderate patients with hemoptysis is useful in terms of low radiation
hemoptysis (> 30 mL/24 hours) or recurrent hemoptysis. exposure, lateralization of bleeding site, and as a screening
Previous reports indicate that the most common cause test for lung disease.
of hemoptysis in Korea was bronchiectasis, followed by Regardless of the amount of hemoptysis, chest CT is
active tuberculosis, and tuberculosis sequelae (5). Possible recommended in patients who have two risk factors for
remaining causes were pneumonia, aspergilloma, lung malignancy (> 40 years old and > 30 pack-year smoking
cancer, others, or unknown (5). CT is more useful than history). Chest CT has the benefit to detect hidden lung
bronchoscopy, because it is noninvasive and accurately cancer that cannot be detected on chest radiography;
assesses the cause and site of hemoptysis; in addition, it however, caution is advised due to radiation exposure.
is also possible to diagnose bronchiectasis, tuberculosis CT is very useful for the simultaneous detection of
and lung cancer with non-contrast-enhanced CT. However, the bleeding site and cause of bleeding in patients with
contrast-enhanced CT is recommended to accurately moderate hemoptysis (> 30 mL/24 hours) or recurrent
assess the bleeding site, because non-bronchial collateral hemoptysis. In Korea, hemoptysis is commonly associated
arteries could be the source of bleeding in tuberculosis with inflammatory diseases that include active tuberculosis
patients despite the bronchial artery being the common and tuberculosis sequelae. In these cases, chest radiography
source of bleeding (13-15). Inoperable massive hemoptysis has several limitations in the evaluation of the bleeding
was considered a major indication of bronchial artery site. CT is therefore very useful for the exact evaluation of

Table 4. Korean Relative Radiation Level


Symbol RRL (mSv) Example
0 0 Sonography, MRI
<1 Chest radiography (PA view), mammography
1−5 IVU, UGIS, low-dose chest CT, brain CT, brain CTA
> 5−10 Routine chest CT, abdominal CT, coronary CT
> 10 3-phase dynamic CT (abdomen)
CT = computed (computer) tomography, CTA = computed tomography angiography, IVU = intravenous urography, MRI = magnetic
resonance imaging, RRL = relative radiation level, PA view = posteroanterior view, UGIS = upper gastrointestinal series. Adapted from
Choi et al. Korean J Radiol 2017;18:208-216 (2).

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Clinical Imaging Guideline for Hemoptysis

bleeding size and causative disease. Rémy J. Multi-detector row CT of hemoptysis. Radiographics
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option in patients with massive hemoptysis, moderate
Usefulness of multi-detector computed tomography before
hemoptysis, or recurrent hemoptysis. CT performed before
bronchoscopy and/or bronchial arterial embolization for
embolization shows a detailed anatomy of both the hemoptysis. Tuberc Respir Dis 2010;68:80-86
bronchial artery and pulmonary artery, helps guide the 7. Revel MP, Fournier LS, Hennebicque AS, Cuenod CA, Meyer
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embolization has significant benefits that outweigh detection of the site and cause of bleeding in patients
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radiation hazards.
2002;179:1217-1224
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8. Delage A, Tillie-Leblond I, Cavestri B, Wallaert B, Marquette
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Supplementary Materials
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cancer incidence in patients with hemoptysis of unknown
The online-only Data Supplement is available with this
origin. Chest 2001;120:1592-1594
article at https://doi.org/10.3348/kjr.2018.19.5.866. 12. Thirumaran M, Sundar R, Sutcliffe IM, Currie DC. Is
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